Skip to main content
NCBI home page
The Journal of General Physiology logoLink to The Journal of General Physiology
. 1990 May 1;95(5):961–979. doi: 10.1085/jgp.95.5.961

Potassium current activated by intracellular sodium in quail trigeminal ganglion neurons

PMCID: PMC2216344  PMID: 2163435

Abstract

Whole-cell voltage clamp and single-channel recordings were performed on cultured trigeminal ganglion neurons from quail embryos in order to study a sodium-activated potassium current (KNa). When KNa was activated by a step depolarization in voltage clamp, there was a proportionality between KNa and INa at all voltages between the threshold of INa and ENa. Single-channel recordings indicated that KNa could be activated already by 12 mM intracellular sodium and was almost fully activated at 50 mM sodium. 100 mM lithium, 100 mM choline, or 5 microM calcium did not activate KNa. The relationship between the probability for the channel to be open (Po) vs. the sodium concentration and the relationship of KNa open time-distributions vs. the sodium concentration suggest that two to three sodium ions bind cooperatively before KNa channels open. KNa channels were sensitive to depolarization; at 12 mM sodium, a 42-mV depolarization caused an e- fold increase in Po. Under physiological conditions, the conductance of the KNa channel was 50 pS. This conductance increased to 174 pS when the intra- and extracellular potassium concentrations were 75 and 150 mM, respectively.

Full Text

The Full Text of this article is available as a PDF (1.1 MB).

Selected References

These references are in PubMed. This may not be the complete list of references from this article.

  1. Bader C. R., Bernheim L., Bertrand D. Sodium-activated potassium current in cultured avian neurones. Nature. 1985 Oct 10;317(6037):540–542. doi: 10.1038/317540a0. [DOI] [PubMed] [Google Scholar]
  2. Bader C. R., Bertrand D., Schlichter R. Calcium-activated chloride current in cultured sensory and parasympathetic quail neurones. J Physiol. 1987 Dec;394:125–148. doi: 10.1113/jphysiol.1987.sp016863. [DOI] [PMC free article] [PubMed] [Google Scholar]
  3. Barrett J. N., Magleby K. L., Pallotta B. S. Properties of single calcium-activated potassium channels in cultured rat muscle. J Physiol. 1982 Oct;331:211–230. doi: 10.1113/jphysiol.1982.sp014370. [DOI] [PMC free article] [PubMed] [Google Scholar]
  4. Bergman C. Increase of sodium concentration near the inner surface of the nodal membrane. Pflugers Arch. 1970;317(4):287–302. doi: 10.1007/BF00586578. [DOI] [PubMed] [Google Scholar]
  5. Bertrand D., Bader C. R. DATAC: a multipurpose biological data analysis program based on a mathematical interpreter. Int J Biomed Comput. 1986 May;18(3-4):193–202. doi: 10.1016/0020-7101(86)90016-4. [DOI] [PubMed] [Google Scholar]
  6. Bertrand D., Cand P., Henauer R., Bader C. R. Fabrication of glass microelectrodes with microprocessor control. J Neurosci Methods. 1983 Feb;7(2):171–183. doi: 10.1016/0165-0270(83)90080-8. [DOI] [PubMed] [Google Scholar]
  7. Byerly L., Meech R., Moody W., Jr Rapidly activating hydrogen ion currents in perfused neurones of the snail, Lymnaea stagnalis. J Physiol. 1984 Jun;351:199–216. doi: 10.1113/jphysiol.1984.sp015241. [DOI] [PMC free article] [PubMed] [Google Scholar]
  8. Bührle C. P., Sonnhof U. Intracellular ion activities and equilibrium potentials in motoneurones and glia cells of the frog spinal cord. Pflugers Arch. 1983 Feb;396(2):144–153. doi: 10.1007/BF00615519. [DOI] [PubMed] [Google Scholar]
  9. Carbone E., Lux H. D. A low voltage-activated, fully inactivating Ca channel in vertebrate sensory neurones. Nature. 1984 Aug 9;310(5977):501–502. doi: 10.1038/310501a0. [DOI] [PubMed] [Google Scholar]
  10. Colburn T. R., Schwartz E. A. Linear voltage control of current passed through a micropipette with variable resistance. Med Biol Eng. 1972 Jul;10(4):504–509. doi: 10.1007/BF02474198. [DOI] [PubMed] [Google Scholar]
  11. Connor J. A., Stevens C. F. Voltage clamp studies of a transient outward membrane current in gastropod neural somata. J Physiol. 1971 Feb;213(1):21–30. doi: 10.1113/jphysiol.1971.sp009365. [DOI] [PMC free article] [PubMed] [Google Scholar]
  12. Dryer S. E., Fujii J. T., Martin A. R. A Na+-activated K+ current in cultured brain stem neurones from chicks. J Physiol. 1989 Mar;410:283–296. doi: 10.1113/jphysiol.1989.sp017533. [DOI] [PMC free article] [PubMed] [Google Scholar]
  13. Galvan M., Dörge A., Beck F., Rick R. Intracellular electrolyte concentrations in rat sympathetic neurones measured with an electron microprobe. Pflugers Arch. 1984 Mar;400(3):274–279. doi: 10.1007/BF00581559. [DOI] [PubMed] [Google Scholar]
  14. Gorman A. L., Thomas M. V. Potassium conductance and internal calcium accumulation in a molluscan neurone. J Physiol. 1980 Nov;308:287–313. doi: 10.1113/jphysiol.1980.sp013472. [DOI] [PMC free article] [PubMed] [Google Scholar]
  15. Grafe P., Rimpel J., Reddy M. M., ten Bruggencate G. Changes of intracellular sodium and potassium ion concentrations in frog spinal motoneurons induced by repetitive synaptic stimulation. Neuroscience. 1982;7(12):3213–3220. doi: 10.1016/0306-4522(82)90243-3. [DOI] [PubMed] [Google Scholar]
  16. HODGKIN A. L., HUXLEY A. F. A quantitative description of membrane current and its application to conduction and excitation in nerve. J Physiol. 1952 Aug;117(4):500–544. doi: 10.1113/jphysiol.1952.sp004764. [DOI] [PMC free article] [PubMed] [Google Scholar]
  17. HODGKIN A. L., KATZ B. The effect of sodium ions on the electrical activity of giant axon of the squid. J Physiol. 1949 Mar 1;108(1):37–77. doi: 10.1113/jphysiol.1949.sp004310. [DOI] [PMC free article] [PubMed] [Google Scholar]
  18. Hamill O. P., Marty A., Neher E., Sakmann B., Sigworth F. J. Improved patch-clamp techniques for high-resolution current recording from cells and cell-free membrane patches. Pflugers Arch. 1981 Aug;391(2):85–100. doi: 10.1007/BF00656997. [DOI] [PubMed] [Google Scholar]
  19. Hartung K. Potentiation of a transient outward current by Na+ influx in crayfish neurones. Pflugers Arch. 1985 May;404(1):41–44. doi: 10.1007/BF00581488. [DOI] [PubMed] [Google Scholar]
  20. Kameyama M., Kakei M., Sato R., Shibasaki T., Matsuda H., Irisawa H. Intracellular Na+ activates a K+ channel in mammalian cardiac cells. Nature. 1984 May 24;309(5966):354–356. doi: 10.1038/309354a0. [DOI] [PubMed] [Google Scholar]
  21. Kato A. C., Rey M. J. Chick ciliary ganglion in dissociated cell culture. I. Cholinergic properties. Dev Biol. 1982 Nov;94(1):121–130. doi: 10.1016/0012-1606(82)90075-6. [DOI] [PubMed] [Google Scholar]
  22. Matsuda H. Open-state substructure of inwardly rectifying potassium channels revealed by magnesium block in guinea-pig heart cells. J Physiol. 1988 Mar;397:237–258. doi: 10.1113/jphysiol.1988.sp016998. [DOI] [PMC free article] [PubMed] [Google Scholar]
  23. Mazzanti M., DiFrancesco D. Intracellular Ca modulates K-inward rectification in cardiac myocytes. Pflugers Arch. 1989 Jan;413(3):322–324. doi: 10.1007/BF00583549. [DOI] [PubMed] [Google Scholar]
  24. Meech R. W. Calcium-dependent potassium activation in nervous tissues. Annu Rev Biophys Bioeng. 1978;7:1–18. doi: 10.1146/annurev.bb.07.060178.000245. [DOI] [PubMed] [Google Scholar]
  25. NARAHASHI T., MOORE J. W., SCOTT W. R. TETRODOTOXIN BLOCKAGE OF SODIUM CONDUCTANCE INCREASE IN LOBSTER GIANT AXONS. J Gen Physiol. 1964 May;47:965–974. doi: 10.1085/jgp.47.5.965. [DOI] [PMC free article] [PubMed] [Google Scholar]
  26. Noma A. ATP-regulated K+ channels in cardiac muscle. Nature. 1983 Sep 8;305(5930):147–148. doi: 10.1038/305147a0. [DOI] [PubMed] [Google Scholar]
  27. Nowycky M. C., Fox A. P., Tsien R. W. Three types of neuronal calcium channel with different calcium agonist sensitivity. Nature. 1985 Aug 1;316(6027):440–443. doi: 10.1038/316440a0. [DOI] [PubMed] [Google Scholar]
  28. Ritchie J. M., Rogart R. B. The binding of saxitoxin and tetrodotoxin to excitable tissue. Rev Physiol Biochem Pharmacol. 1977;79:1–50. doi: 10.1007/BFb0037088. [DOI] [PubMed] [Google Scholar]
  29. Sakmann B., Trube G. Conductance properties of single inwardly rectifying potassium channels in ventricular cells from guinea-pig heart. J Physiol. 1984 Feb;347:641–657. doi: 10.1113/jphysiol.1984.sp015088. [DOI] [PMC free article] [PubMed] [Google Scholar]
  30. Schwindt P. C., Spain W. J., Crill W. E. Long-lasting reduction of excitability by a sodium-dependent potassium current in cat neocortical neurons. J Neurophysiol. 1989 Feb;61(2):233–244. doi: 10.1152/jn.1989.61.2.233. [DOI] [PubMed] [Google Scholar]
  31. Storm J. F. Temporal integration by a slowly inactivating K+ current in hippocampal neurons. Nature. 1988 Nov 24;336(6197):379–381. doi: 10.1038/336379a0. [DOI] [PubMed] [Google Scholar]

Articles from The Journal of General Physiology are provided here courtesy of The Rockefeller University Press

RESOURCES